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Adaptive threonine increase in transmembrane regions of mitochondrial proteins in higher primates.

Kitazoe Y, Kishino H, Hasegawa M, Nakajima N, Thorne JL, Tanaka M - PLoS ONE (2008)

Bottom Line: This Thr increase involved the replacement of hydrophobic AAs in the membrane interior.Because crucial roles of Thr and Ser in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in the higher primates might be adaptive by serving to reinforce stability of mt proteins in the inner membrane.The correlation between Thr composition in the membrane interior and the longevity of animals is striking, especially because some mt functions are thought to be involved in aging.

View Article: PubMed Central - PubMed

Affiliation: Center of Medical Information Science, Kochi Medical School, Nankoku, Kochi, Japan. kitazoey@kochi-u.ac.jp

ABSTRACT

Background: The mitochondrial (mt) gene tree of placental mammals reveals a very strong acceleration of the amino acid (AA) replacement rate and a change in AA compositional bias in the lineage leading to the higher primates (simians), in contrast to the nuclear gene tree. Whether this acceleration and compositional bias were caused by adaptive evolution at the AA level or directional mutation pressure at the DNA level has been vigorously debated.

Methodology/principal findings: Our phylogenetic analysis indicates that the rate acceleration in the simian lineage is accompanied by a marked increase in threonine (Thr) residues in the transmembrane helix regions of mt DNA-encoded proteins. This Thr increase involved the replacement of hydrophobic AAs in the membrane interior. Even after accounting for lack of independence due to phylogeny, a regression analysis reveals a statistical significant positive correlation between Thr composition and longevity in primates.

Conclusion/significance: Because crucial roles of Thr and Ser in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in the higher primates might be adaptive by serving to reinforce stability of mt proteins in the inner membrane. The correlation between Thr composition in the membrane interior and the longevity of animals is striking, especially because some mt functions are thought to be involved in aging.

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Related in: MedlinePlus

Hoa→Thr flow along the primate lineage.Figures A, B and C represent, respectively, the increased number in Thr, the decreased number in Hoa (relative to the Thr/Hoa numbers of the root sequence) and the evolutionary rate, as functions of the divergence times of primates. The evolutionary rate was traced along the human lineage. The values of the times and rates were estimated using a harmonic mean method which is robust against strong evolutionary rate changes [20]. Here, we used the root and node AA sequences which were obtained in Figure 1.
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pone-0003343-g002: Hoa→Thr flow along the primate lineage.Figures A, B and C represent, respectively, the increased number in Thr, the decreased number in Hoa (relative to the Thr/Hoa numbers of the root sequence) and the evolutionary rate, as functions of the divergence times of primates. The evolutionary rate was traced along the human lineage. The values of the times and rates were estimated using a harmonic mean method which is robust against strong evolutionary rate changes [20]. Here, we used the root and node AA sequences which were obtained in Figure 1.

Mentions: By chronologically tracing the greatest flow along the simian lineage, we detect a strong correlation between the decrease in Hoa and the increase in Thr (Figure 2A and B). The tree shrew lineage, with a very short branch (Figure 1), had a minimal flow, and the loris lineage, with a moderately long branch, had a small flow. We also observe that the Hoa→Thr flow is associated with an accelerated AA evolutionary rate (Figure 2C) in the early stages of primate evolution previously reported [20]. This observation seems to be consistent with the higher rates of nonsynonymous relative to synonymous substitutions that occurred in complexes IV (cytochrome c oxidase subunits) [5]–[9]. By applying the flow analysis to each protein, we found that the Hoa→Thr flow was generally large in complexes I (NADH dehydrogenase subunits 1, 2, 4 & 5; ND1, ND2, ND4 & ND5) and III (cytochrome b; Cytb), and rather small in complexes IV (cytochrome c oxidase subunits) and V (ATPase subunits). We note that ND2 displayed a Hoa→Ser flow in addition to the Hoa→Thr flow.


Adaptive threonine increase in transmembrane regions of mitochondrial proteins in higher primates.

Kitazoe Y, Kishino H, Hasegawa M, Nakajima N, Thorne JL, Tanaka M - PLoS ONE (2008)

Hoa→Thr flow along the primate lineage.Figures A, B and C represent, respectively, the increased number in Thr, the decreased number in Hoa (relative to the Thr/Hoa numbers of the root sequence) and the evolutionary rate, as functions of the divergence times of primates. The evolutionary rate was traced along the human lineage. The values of the times and rates were estimated using a harmonic mean method which is robust against strong evolutionary rate changes [20]. Here, we used the root and node AA sequences which were obtained in Figure 1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2553178&req=5

pone-0003343-g002: Hoa→Thr flow along the primate lineage.Figures A, B and C represent, respectively, the increased number in Thr, the decreased number in Hoa (relative to the Thr/Hoa numbers of the root sequence) and the evolutionary rate, as functions of the divergence times of primates. The evolutionary rate was traced along the human lineage. The values of the times and rates were estimated using a harmonic mean method which is robust against strong evolutionary rate changes [20]. Here, we used the root and node AA sequences which were obtained in Figure 1.
Mentions: By chronologically tracing the greatest flow along the simian lineage, we detect a strong correlation between the decrease in Hoa and the increase in Thr (Figure 2A and B). The tree shrew lineage, with a very short branch (Figure 1), had a minimal flow, and the loris lineage, with a moderately long branch, had a small flow. We also observe that the Hoa→Thr flow is associated with an accelerated AA evolutionary rate (Figure 2C) in the early stages of primate evolution previously reported [20]. This observation seems to be consistent with the higher rates of nonsynonymous relative to synonymous substitutions that occurred in complexes IV (cytochrome c oxidase subunits) [5]–[9]. By applying the flow analysis to each protein, we found that the Hoa→Thr flow was generally large in complexes I (NADH dehydrogenase subunits 1, 2, 4 & 5; ND1, ND2, ND4 & ND5) and III (cytochrome b; Cytb), and rather small in complexes IV (cytochrome c oxidase subunits) and V (ATPase subunits). We note that ND2 displayed a Hoa→Ser flow in addition to the Hoa→Thr flow.

Bottom Line: This Thr increase involved the replacement of hydrophobic AAs in the membrane interior.Because crucial roles of Thr and Ser in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in the higher primates might be adaptive by serving to reinforce stability of mt proteins in the inner membrane.The correlation between Thr composition in the membrane interior and the longevity of animals is striking, especially because some mt functions are thought to be involved in aging.

View Article: PubMed Central - PubMed

Affiliation: Center of Medical Information Science, Kochi Medical School, Nankoku, Kochi, Japan. kitazoey@kochi-u.ac.jp

ABSTRACT

Background: The mitochondrial (mt) gene tree of placental mammals reveals a very strong acceleration of the amino acid (AA) replacement rate and a change in AA compositional bias in the lineage leading to the higher primates (simians), in contrast to the nuclear gene tree. Whether this acceleration and compositional bias were caused by adaptive evolution at the AA level or directional mutation pressure at the DNA level has been vigorously debated.

Methodology/principal findings: Our phylogenetic analysis indicates that the rate acceleration in the simian lineage is accompanied by a marked increase in threonine (Thr) residues in the transmembrane helix regions of mt DNA-encoded proteins. This Thr increase involved the replacement of hydrophobic AAs in the membrane interior. Even after accounting for lack of independence due to phylogeny, a regression analysis reveals a statistical significant positive correlation between Thr composition and longevity in primates.

Conclusion/significance: Because crucial roles of Thr and Ser in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in the higher primates might be adaptive by serving to reinforce stability of mt proteins in the inner membrane. The correlation between Thr composition in the membrane interior and the longevity of animals is striking, especially because some mt functions are thought to be involved in aging.

Show MeSH
Related in: MedlinePlus